Download The potential role of waterbirds in dispersing invertebrates and

The potential role of waterbirds in dispersing invertebrates and plants
in arid Australia
A.J.GREEN*, K.M. JENKINS†‡, D. BELL§, P.J. MORRIS† AND R.T. KINGSFORD‡
* Department of Wetland Ecology, Estación Biológica de Doñana-CSIC, Avda. María
Luisa s/n, Pabellón del Perú, 41013 Sevilla, Spain
† Ecosystem Management, University of New England, Armidale, NSW, Australia
§ Botany, University of New England, Armidale, NSW, Australia
‡ School of Biological, Earth and Environmental Sciences, University of New South
Wales, Sydney, NSW, Australia
Keywords: arid-zone river, nomadic waterfowl, passive dispersal, propagules,
temporary wetlands.
Running title: Arid-zone dispersal of propagules by waterbirds
Correspondence: Dr. A.J. Green, Department of Wetland Ecology, Estación Biológica
de Doñana-CSIC, Avda. María Luisa s/n, Pabellón del Perú, 41013 Sevilla, Spain.
Email: [email protected]
Author Posting. This is the author’s version of the work. It is posted here for personal
use, not for redistribution. The definitive version was published in Freshwater Biology
53: 380-392. (2008: doi:10.1111/j.1365-2427.2007.01901.x)
.
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SUMMARY
1. The role of waterbirds as vectors of plants and invertebrates within and between aridzone wetlands is poorly understood. We present the first detailed study of passive
dispersal by nomadic birds in Australasia. We investigated the numbers and types of
invertebrate and plant propagules within freshly collected faecal samples as well as their
viability. We compared dispersal among Grey Teal (Anas gracilis), Eurasian Coot
(Fulica atra) and Black Swan (Cygnus atratus) in the Macquarie Marshes, a complex of
temporary to semi-permanent wetlands in New South Wales.
2. When faecal samples (n = 60) were inundated in the laboratory and monitored over
three weeks, ciliates (75% of samples), nematodes (22%), ostracods (13%) and rotifers
(5%) were recorded, with higher taxon richness in coot samples. Faecal samples (n =
71) were also sieved to quantify intact propagules, and ostracod eggs (70% of samples),
large branchiopod eggs (31%) and bryozoan statoblasts (31%) were the most abundant
invertebrates. Diaspores of 19 plant taxa were recorded, 14 of which were germinated in
the laboratory or shown to be viable at the end of germination trials. The abundance and
diversity of invertebrate propagules was highest in coot samples, whereas the abundance
and diversity of diaspores was highest in teal samples.
3. One Australian Pelican (Pelecanus conspicillatus) sample was obtained and found to
contain more taxa and far more propagules than any sample from other waterbirds,
suggesting that piscivorous birds might have an important role in the indirect dispersal
of propagules ingested by fish.
4. Our results support a role for birds in explaining the distributions of cosmopolitan
plant genera such as Lemna, Typha, Myriophyllum and Nitella. The alien plants
Ranunculus sceleratus, Medicago polymorpha and Polygonum arenastrum were
recorded, demonstrating the potential role of waterfowl in the spread of exotic species.
As the frequency and duration of flooding of arid-zone wetlands decreases owing to
human activities, the importance of waterbirds in facilitating recolonisation of
temporary wetlands is likely to increase.
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Introduction
Temporary wetlands are the dominant wetland type in arid zones of Australia and other
continents, but vary greatly in their frequency, duration and timing of flooding (Boulton
& Brock, 1999; Porter et al., 2001). Many aquatic plants and zooplankton survive
intervening drought periods as dormant stages in long-lived propagule banks (Roshier et
al., 2001; Brock et al., 2003; Boulton et al., 2006; Jenkins & Boulton, 2007), or
recolonise temporary arid-zone wetlands via hydrological connections, especially via
floodwaters entering from rivers (Jenkins & Boulton, 2003). In addition, waterbirds can
potentially transport plants and invertebrates between wetlands (Figuerola & Green,
2002a; Green et al., 2002), although there is little information on the importance of such
waterbird vectors in temporary wetlands.
In arid Australia, waterbird populations undergo boom and bust cycles and
regular nomadic movements in response to the unpredictable changes in surface area
and distribution of temporary wetlands suitable for feeding and breeding (Kingsford et
al., 1999; Kingsford & Norman, 2002; Roshier et al., 2002). In more seasonal Holarctic
environments, strictly migratory waterfowl (Anatidae and coot) are major dispersers of
seeds and invertebrates between wetlands (Proctor, 1964; Holt-Mueller & Van der Valk,
2002; Figuerola et al., 2003). In this study in inland south-east Australia, we
investigated what plants and invertebrates are transported by nomadic waterbird species
in their digestive systems. We aimed to identify and quantify propagules excreted by
waterfowl, and to assess their viability through emergence and germination
experiments. We compared the importance as vectors of ducks feeding in the sediments
of flooded wetlands with that of grazing waterfowl. We also investigated whether fisheating birds might indirectly disperse plant or invertebrate propagules, as proposed by
Darwin (1859).
Methods
Collection of faecal samples
Samples of waterbird faeces were collected from the Macquarie Marshes in New South
Wales on 27-28 July 2005. The Macquarie Marshes (30o35´S, 147o32´E) are a complex
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of floodplain, lagoons and creeks (200,000 ha) with water regimes ranging from
temporary to permanent (Paijmans, 1981). They are partly protected as a Ramsar site
but are severely impacted by upstream dams and water extraction (Kingsford & Thomas
1995, Kingsford & Johnson 1998). Water levels were low at the time of our visit, and
samples were collected from two semi-permanent lagoons where waterbirds
concentrated; Buckuyinguy Swamp (31o02’S, 147o28’E) and Stock Lagoon (31o05’S,
147o30’E), separated from each other by 2 km.
Sixty Grey Teal (Anas gracilis Buller) faecal samples were collected from
Buckuyinguy Swamp, 30 Eurasian Coot (Fulica atra Linnaeus) faecal samples were
collected from Stock Lagoon, and 30 Black Swan (Cygnus atratus Latham) faecal
samples were collected from both lagoons and flooded grassland located between them.
One Australian Pelican (Pelecanus conspicillatus Temminck) sample was collected
from Stock Lagoon. At the time of the sampling, approximately 150 teal, 150 coots, 200
swans and one pelican were in the study area. Teal were present at Stock Lagoon, but
did not frequent accessible banks where faeces could be collected. The conductivity of
water at Buckuyinguy Swamp was 362-440 μS cm-1 (n = 4), and at Stock Lagoon was
522-737 μS cm-1 (n = 4). Although Black Swans and coot have been classified as deepwater foragers (Roshier et al., 2002), during our study they were grazing at the water’s
edge and out of the water in grassland. Teal were dabbling in the water column or in the
sediments in the shallow parts of the lagoons.
Fresh faeces were collected from areas where monospecific flocks of birds were
observed feeding or roosting out of the water. Each of the four species studied produced
droppings with a distinctive size and colour. Fresh weight for each sample was 1.33 ±
0.11 g (mean ± s.e., n = 16) for coot, 1.37 ± 0.07 g (n = 32) for teal, 10.5 ± 0.77 g (n =
23) for swans and 26.4 g for the pelican. The pelican sample was collected in the late
afternoon from a log where the bird had roosted through the day. Samples from the
other three species were collected from short, grazed grass and were usually not in
contact with soil. Any part of the dropping in contact with soil was removed with a
penknife and discarded to avoid contamination. It is unlikely that any individual bird
was sampled more than once. Droppings collected were separated by at least 1 m. Each
dropping was sealed in a plastic tube, then kept in a cool box with ice until we reached
the laboratory at the University of New England.
Emergence of invertebrates from faeces
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On 30 July 2006, about 0.3 g fresh weight from each of 30 grey teal, 15 Eurasian coot
and 15 black swan samples was placed in a 70 cm3 vial together with 20 cm3 of mineral
water (conductivity 467 μS cm-1) to permit hatching of viable resting eggs. The lid was
placed loosely on each vial to allow air exchange while reducing evaporation and the
risk of aerial contamination by propagules. Ten controls were established with mineral
water only, and ten (five from each lagoon) with mineral water and a similar quantity of
the same type of shoreline vegetation (grasses) upon which most of the droppings had
been deposited by the birds. Vials were randomly placed on the laboratory bench with a
natural light schedule and temperatures oscillating from 15oC at night to 25oC during
the day. The presence of live invertebrates was recorded for all vials using a binocular
microscope (Leica MZ8, 10-50 x) on days 1, 3, 7, 14 and 21 after inundation. Total
counts of invertebrates were made, except for abundance of protozoans that were
estimated in the following abundance classes; 1-2, 3-10, 11-20, 21-50, 51-100, 101-200,
201-500, 501-1000, 1001-2000, 2001-5000, 5001-10000 and > 10000 per sample.
However, since numbers may have been increased by reproduction after hatching, here
we only present data on the presence or absence of each taxon in each sample.
Sieving for aquatic propagules
Remaining faecal samples were stored in the dark in a refrigerator at 2oC. Between 15
August and 20 September, we washed 30 teal, 20 coot and 20 swan samples and the one
pelican sample through stacked 1 mm, 250 µm and 63 µm sieves using reverse osmosis
water. Most of these faecal samples (27 of the teal, 14 of the coot and 14 of the swan
samples) were the same ones used in the hatching experiment (i.e. we sieved that part of
the sample remaining after removing part for the hatching experiment). Owing to their
larger size, only 73.5 ± 5.1 % by fresh weight (mean ± s.e., range 44-100%, n = 20) of
swan samples and 51% of the pelican sample were sieved for propagules. Items retained
on the sieves were placed in sample trays and inspected using a binocular microscope,
removing apparently intact invertebrate propagules or plant diaspores that were then
sorted and placed in tubes with a mixture of mineral water and reverse osmosis water.
Eggs were returned to the refrigerator until they were measured, photographed and
identified to the highest taxonomic resolution possible with the help of experts. Some
were placed in filtered water from a nearby dam in Petri dishes at room temperature and
any daily development observed. Photographs of eggs are available on request.
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Germination from plant diaspores
We use the term diaspores from hereon as the plant dispersal units we recorded in
faeces included fruits (e.g. Cyperaceae), mericarps (Myriophyllum) and oogonia
(Nitella) as well as seeds (see results). Diaspores recovered from sieving were viewed
under a binocular microscope for initial identification and assessment. Intact diaspores
were placed in 30 ml of tap water in 6.5 cm diameter Petri dishes and incubated in
germination cabinets set to 12 h of light at 25 ºC and 12 h of darkness at 15 ºC. Light
was provided by fluorescent tubes emitting an intensity of 35 µE m-2 s-1 over the diurnal
cycle. Emerging seedlings were potted into standard potting mix and grown in a
glasshouse for identification. Where seedlings could not be successfully established,
seeds were identified by comparing them with those on herbarium specimens at the
NCW Beadle Herbarium UNE, or in the case of Lemna disperma Hegelm from
published photographs of seeds (Cross, 2006). When germination trials were completed
after about six months, all remaining diaspores were crushed to assess whether or not
they were viable. Although most diaspores were rotten by then (see results), as well as
data on the numbers of germinating and viable seeds, we present the total numbers of
diaspores which appeared intact and potentially viable when initially extracted from
faeces. We consider this justified because many diaspores rotten at the end of the study
may have been viable at the moment of collection. Furthermore, these total numbers are
more comparable with other studies of avian dispersal, which did not separate
apparently whole seeds into viable and non-viable groups (e.g. Holt-Mueller & Van der
Valk, 2002; Figuerola et al., 2003; Charalambidou & Santamaria, 2005).
Statistics
We used 2x3 Fisher Exact tests (Lowry, 2006) to examine differences in the presence
and absence of emerging invertebrates among teal, coot and swans. Chi-squared tests
were not used owing to the high proportion of cells with expected values below five.
We considered a taxon as present in a sample when it was recorded on at least one of
the five days it was inspected. 2x2 Fisher Exact tests (StatSoft, 2001) were used to
conduct pairwise post-hoc comparisons when significant differences between groups
were recorded.
Owing to the abundance of zero values, we used non-parametric Kruskal-Wallis
tests to compare the abundance and taxa richness of sieved propagules among teal, coot
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and swans (StatSoft, 2001). Mann-Whitney U tests were used to conduct pairwise posthoc comparisons when significant differences among groups were recorded.
Results
Emergence of invertebrates
Protozoans (ciliates), nematodes, ostracods and three rotifer taxa emerged from
inundated waterfowl droppings (Table 1). No invertebrates emerged from any of the
control samples, either those with water only or those with grass plus water. Protozoans
were the group recorded in the highest proportion of samples, occurring in 83% of teal,
87% of coot and 47% of swan samples (Table 1, Fig. 1). These differences between bird
species were significant (2x3 Fisher Exact test, P = 0.029). Post-hoc tests showed that
the presence of protozoa was significantly lower in swan samples than in those from
teal (P = 0.016) or coot (P = 0.050).
Nematodes were recorded in 60 % of coot, 20% of swan but only 3% of teal
samples. These differences between species were highly significant (P < 0.0001). Posthoc tests showed that the presence of nematodes was significantly lower in teal samples
than in coot (P < 0.0001). Ostracods were recorded in 33 % of coot but only 7% of
swan and teal samples, but these differences were not significant (P = 0.055). Two
ostracod taxa were identified in our samples (S. Halse pers. comm.). The most abundant
taxon (Cyprinotus sp.) was up to 1.7 mm in length with a pale orange colour. A much
smaller number of Cypretta sp. were observed, with a hairy and pitted valve surface and
dark green coloration.
Rotifers were absent from teal samples but recorded in 7% of swan samples and
13% of coot samples. These differences were not significant (P = 0.12).
Invertebrate propagules found by sieving
Numbers of invertebrate propagules (Kruskal-Wallis test, H2,70 = 9.94 p <0.007) and
numbers of invertebrate taxa (H2,70 = 8.29 p = 0.016) in faecal samples were
significantly different among coot, teal and swans (Fig. 2). Coot samples contained
significantly more propagules and more invertebrate taxa than swans or teal (Fig. 2), as
confirmed by post-hoc tests (P < 0.04). However, the pelican sample contained as many
taxa (5) and six times as many propagules as any other waterbird sample (Table 2). The
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relative abundance of different taxa varied among bird species (Table 2). In particular,
teal samples contained relatively more large branchiopod eggs and fewer bryozoan
statoblasts than did swan and coot samples.
Ostracod cf eggs were soft and irregular in shape, 120-160 µm in diameter and
pink-orange in colour. They were found both individually and in clusters of two to eight
eggs, sometimes attached to fragments of vegetation. Their viability was confirmed
when eggs left at room temperature developed two dark red, squarish eye spots within a
week then a pair of legs or antennae within the egg within three more days. By that
time, these latter structures had a dark pink outline but most of the egg was whitish and
had lost its colour. These eggs were particularly abundant in coot samples (Table 2),
supporting the view that they were ostracod eggs since ostracods (mainly Cyprinotus
sp.) hatched with a higher frequency from coot samples (Table 1, Fig. 1).
Large branchiopod eggs were likely to be of Branchinella sp. (Anostraca, S.
Halse pers. comm.) and were distinct brown or orange spheres or flattened spheres,
typically 200-320 µm in diameter. Given their abundance in teal samples (Table 2), they
were probably concentrated in sediments.
Bryozoan statoblasts were 360-440 µm in length and were floatoblasts
belonging to an undescribed species of Plumatella (T.S. Wood pers. comm.). Their
viability was confirmed when one of six statoblasts from the same coot sample placed at
room temperature on 13/9/05 hatched after three days.
We could not satisfactorily divide cladoceran ephippia into different taxa,
although it is likely that around four taxa were recorded. All but four ephippia had a
single egg case, their length varying from 400-1200 µm. Double ephippia were 10001400 µm long and were likely to be of Daphnia carinata King (R. Shiel pers. comm.).
We were unable to hatch any ephippia. Chydorids were often recorded intact but dead
when faeces were sieved.
Plant diaspores
Intact diaspores of 19 plant taxa were recovered by sieving faecal samples, including 12
identified to species (Table 3). Germination was recorded in nine taxa, and another five
taxa remained viable at the end of the germination trials (Table 4). Total numbers of
diaspores (Kruskal-Wallis test, H2,70 = 25.71 P <0.0001) and numbers of taxa (H2,70 =
24.44 P < 0.0001) in faecal samples were significantly different among coot, teal and
swans (Fig. 3). This was because teal samples contained both significantly more
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diaspores and more plant taxa than swans and coot (Fig. 3), as confirmed by post-hoc
tests (P < 0.0001). However, the pelican sample contained more taxa and more than
four times as many diaspores as any other waterbird sample (Table 3, Fig 3).
The relative abundance of different taxa varied among bird species (Table 3).
The majority (62%) of diaspores found in teal samples were Cyperaceae, yet this family
was not recorded in other birds. Many of the Cyperaceae diaspores had a black colour
typical of those that have spent some time within sediments. Ranunculus seeds were
recorded in 27% of teal samples, but were absent in other birds. Typha was the most
abundant genus recorded in the single pelican sample and in swan samples, yet was
absent in the teal samples. There was a striking similarity in the taxa recorded in coot
and pelican samples, although abundance was much higher in the pelican sample.
Larger diaspores with a length exceeding 1 mm were almost exclusively recorded in teal
samples (Table 3).
Swan samples were dominated by shreds of grass leaves. Swan and especially
coot samples contained large amounts of Azolla filiculoides Lamarck tissue, including
clusters containing massulae and megasporocarps, some of which were potentially
viable. Teal samples contained large amounts of live filamentous algae. Neither the
algae nor the Azolla were quantified in our sieved samples. However, live filamentous
algae were recorded in 43% of teal samples and 7% of swan samples during the
emergence experiment.
Three alien species survived gut passage. Celery-leaved buttercup (Ranunculus
sceleratus Linnaeus) seeds were in eight teal samples, one Burclover (Medicago
polymorpha Linnaeus) seed was in a swan sample, and four oval-leaf knotweed
(Polygonum arenastrum Boreau) seeds were in a swan sample (Table 3). Eight R.
sceleratus seeds and one P. arenastrum seed germinated, whereas the M. polymorpha
seed remained viable at the end of the germination trials (Table 4).
Discussion
Dispersal of propagules by waterbirds
As far as we are aware, this is the first field study of internal dispersal by waterfowl to
simultaneously identify and test the viability of both invertebrate and plant taxa. The
only previous field study of internal transport by Australian waterbirds was limited to
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dispersal of Eleocharis by the relatively sedentary Purple Gallinule (Porphyrio
porphyrio Linnaeus) in lakes of the Great Dividing Range in the New England
tablelands (Bell, 2000).
Invertebrates emerged from 82% of our waterbird faecal samples in our hatching
experiment, and we sieved invertebrate propagules or plant diaspores from 85% and
59% of our samples respectively. Each sample only held a small proportion of the daily
faecal output for each bird. For example, since the daily faecal output for black swans is
around 418 g fresh weight per day (Mitchell & Wass, 1995), each sample for the
hatching experiment contained about 0.1% of daily output, and each sample sieved
contained about 2%. Thus, our results show the great potential for colonisation of
temporary wetlands by invertebrates and plants transported internally by birds.
Dispersal of propagules externally on feet or in plumage is also likely to be important
(Figuerola & Green, 2002a,b). When invertebrates, aquatic plants and waterfowl
numbers increase greatly after flooding (Kingsford et al., 1999; Boulton et al., 2006;
Brock et al., 2006), there is potential for massive transport of invertebrates and plants.
The species in this study and most other Australian waterbirds are highly dispersive
and nomadic (Marchant & Higgins, 1990; Kingsford & Norman, 2002; Roshier et al.,
2002). For example, grey teal can disperse up to 343 km in a day (Roshier et al., 2006),
enough to gradually spread plants or invertebrates between temporary wetlands over
huge areas of arid Australia given the high levels of avian connectivity between
wetlands at times of peak floods (Roshier et al., 2001). All four waterfowl species
studied have a continental distribution, while teal and pelicans occasionally move from
Australia to neighbouring parts of Asia (Tracey et al., 2004). Experimental data on
retention times (Charalambidou & Santamaría, 2002; Holt-Mueller & Van der Valk,
2002; Charalambidou et al., 2003b; Pollux et al., 2005) suggest that invertebrates and
plant diaspores can readily be transported in the gut of waterfowl for several hundred
km. For example, the Bewick’s Swan Cygnus columbianus Ord is a similar size to the
Black Swan and has a retention time between 2.5 and 8 h when feeding on grass (B.
Nolet pers. comm.) and a flight speed of 72 km/h (Welham, 1994).
Many of the birds we studied probably moved away from the Macquarie Marshes
within days of our visit, or after heavy rains arrived the following month (Roshier et al.,
2002), spreading plants and invertebrates between wetlands. Waterbirds would also
disperse these organisms within different parts of the extensive Macquarie Marshes,
especially when inundated. However, if propagules of a given species are transported by
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birds to new habitats, they may not become established there. Differences in the
composition of aquatic communities are often better explained by local processes
(competition, predation, differences in environmental conditions, etc) than by regional
processes such as dispersal limitation (Langley et al., 2001; Cottenie et al., 2003). Our
results suggest that such local processes explain the marked dissimilarity of community
composition among closely neighbouring Australian wetlands (Brock et al., 2003).
Since no invertebrates hatched in our controls, we are confident that our results are
not seriously affected by contamination of propagules from bankside vegetation or from
the air. Many propagules were clearly visible within the interior of the faecal samples. It
is possible that higher rates of emergence from faecal samples in the hatching trials
would have been recorded by maintaining them at lower temperatures than those used
(Vandekerkhove et al., 2005) or oxygenating the samples. The large branchiopod eggs
did not hatch because they did not undergo the period of desiccation required to break
diapause, although it is likely that many remained viable after gut passage (Sánchez et
al., 2007).
Migratory waterfowl in the northern hemisphere transport ciliates, ostracods,
cladocerans, rotifers and nematodes internally (Green & Figuerola, 2005; Frisch et al.,
2007). Bryozoan statoblasts occur in faeces from a variety of European migratory
waterfowl (Figuerola et al., 2003; Figuerola et al., 2004), and we confirmed their
viability (see also Charalambidou et al., 2003a). Waterbirds are widely assumed only to
be important vectors for invertebrates with resistant, diapause eggs (e.g. Bilton et al.,
2001), yet we observed large numbers of apparently viable non-diapause ostracod eggs.
Thus, egg morphology should not be considered a reliable indicator of avian dispersal
potential (see also Bartholme et al., 2005; Green & Sánchez, 2006).
Differing dispersal potential between waterbirds
Among the three main waterbird species, teal had a higher diversity and abundance of
plant diaspores, whereas coot had a higher diversity and abundance of invertebrate
propagules (as indicated both by sieving and hatching). Teal probably excreted more
plant diaspores and large branchiopod eggs because they ingested them from the seed
and egg bank when feeding in submerged sediments. In contrast, coot were mainly
grazing on aquatic vegetation at the water’s edge, and probably ingested many
invertebrate propagules attached to this vegetation or floating at the water’s edge. For
example, the ostracod eggs were often attached to fragments of vegetation within the
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faeces, and the Plumatella floatoblasts are likely to have been floating when ingested.
Observed differences between waterfowl species may also be partially explained by
differences in digestive efficiency. For example, invertebrate propagules may have had
higher survival when passing through the digestive tract of herbivorous coot and swans,
owing to lower efficiency digesting animal matter compared to omnivorous teal
(Charalambidou et al., 2005).
However, coot and teal samples were collected from different lagoons, and
differences between sites in abundance of propagules may have contributed to
differences among bird species. Invertebrate community composition in epibenthic
cores taken at the time of our study (includes 1 cm mud and 250 ml water; see King
2004 for method) differed between the lagoons, with ostracods and Brachionus rotifers
more common in Stock Lagoon, where the coot were feeding (authors, unpublished
data). These taxa emerged more frequently from coot faeces. However, these lagoons
were similar in total microinvertebrate densities (232 individuals/core at Buckuyinguy
and 171 at Stock), water chemistry, habitat structure and composition, and both coot
and teal samples were significantly different in propagule composition from the swan
samples taken from both lagoons. Thus, differences between the lagoons cannot explain
all the differences recorded between waterfowl species.
If bill morphology were all-important in determining which waterfowl species make
good vectors, we would predict that teal would have both more plant and invertebrate
propagules in their faeces. Their relatively dense lamellae in their bill for filtering food
should favour ingestion of small particles, including propagules (Crome, 1985; Green &
Figuerola, 2005). In contrast, we have found teal to be particularly important vectors of
larger seeds, which are a major component of their diet (Marchant & Higgins, 1990).
Evidently, in the absence of information on the spatial distribution of propagules,
neither feeding method nor bill morphology reliably predict the importance of different,
sympatric waterfowl species as dispersal vectors (see Green et al., 2002 for further
discussion). However, grazing waterfowl such as swans, coot and geese appear to be
particularly good dispersers of Plumatella floatoblasts (Figuerola et al., 2004).
Dispersal of alien and cosmopolitan plants
As far as we know, our study is the first to demonstrate that the cosmopolitan plant
genera Lemna, Typha, Myriophyllum and Nitella are transported internally by
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waterbirds. Given their ability to reproduce vegetatively from fragments, Lemna, Typha
and Myriophyllum may also be dispersed externally on the feet or plumage of waterfowl
(Sawada et al., 2003). Lemna has been seen to be carried on the backs of waterfowl
(Darwin 1859), but we are not aware of such direct evidence for Typha or
Myriophyllum. Duckweeds have previously been assumed not to be seed-dispersed (Les
et al. 2003), but we found Lemna seeds in faeces from three bird species. Molecular
evidence strongly suggests that long-distance dispersal by birds over evolutionary
timescales explains the cosmopolitan distribution of aquatic genera such as Lemna and
Myriophyllum (Les et al., 2003). Our findings suggest that diaspores transported
internally may be more readily transported over long distances than vegetative parts
carried externally and prone to desiccation. Typha seeds are generally assumed to be
dispersed by wind (Cain et al., 1998), but we found viable seeds in three bird species,
suggesting that birds can be a main means of long-distance dispersal for seeds
morphologically adapted for wind dispersal (Higgins et al., 2003; Sánchez et al., 2006).
Our results demonstrate the potential importance of waterbirds (sensu Wetlands
International 2002) as vectors of alien plants (see also Powers et al., 1978). All three of
the exotic species we recorded are widespread and expanding in Australia (Western
Australian Herbarium, 1998; DWBLC, 2005; Martin et al., 2006) and are invasive in
the USA (USDA-NRCS, 2007). M. polymorpha and P. arenastrum are not confined to
wetlands, so waterbirds can disperse terrestrial alien plants as well as aquatic ones (see
also Sánchez et al., 2006). Wetland associated exotic plants can also be dispersed by
terrestrial birds (Renne et al., 2000).
Indirect dispersal by fish-eating birds
Darwin (1859) explicitly recognised that fish-eating birds may disperse propagules
ingested by fish between different wetlands, yet this process has not previously been
corroborated (but see Mellors, 1975). Our pelican sample contained over four times as
many plant diaspores and six times as many invertebrate propagules as any other
sample, even though we only sieved half of it. All the propagules were relatively small,
and probably came from the gut contents of small fish. Such a large quantity of
propagules was unlikely to be ingested incidentally (e.g. from sediments or water).
Lemna and Typha seeds from pelican faeces were germinated, confirming that this
nomadic fish-eater disperses plants. Such indirect or secondary dispersal also occurs in
terrestrial systems (Nogales et al., 2002). Future work should address indirect dispersal
13
by fish-eating birds, and assess its importance compared with that of waterfowl,
shorebirds and other waterbirds (see Figuerola & Green, 2002a; Green et al., 2002;
Green & Figuerola, 2005 for reviews of dispersal by these latter groups).
Conclusion
This study extends our knowledge of the extraordinary role of waterbirds in
connecting other organisms across wetlands that fluctuate in space and time. Birds are
likely to be particularly important in facilitating the recolonization of invertebrates and
plants with limited drought resistance in temporary wetlands after reflooding. The
importance of this role is likely to be increasing over time as dam construction,
extraction for agriculture and global warming cause the hydroperiods of Australian
wetlands to decrease and the intervals between flooding events that physically connect
different wetlands to increase (Kingsford & Johnson, 1998; Jenkins et al., 2005).
Acknowledgements
We thank the Thornton family for allowing us to conduct research in the study area, and
A. Boulton for helpful discussions. The Australian Research Council APDI fellowship
and Linkage grant (LP0453694), Department of Environment and Conservation,
Department of Natural Resources, University of New England supported this research.
The first author was supported by a three-month stipend from the mobility programme
of the Spanish Ministry of Education and Science (PR2005-0183). S. Halse, J. McRae,
B. Nolet, R. Shiel, D. Roshier and T.S. Wood provided helpful information.
References
Bartholme, S., Samchyshyna, L., Santer, B. & Lampert, W. (2005) Subitaneous eggs of
freshwater copepods pass through fish guts: survival, hatchability, and potential
ecological implications. Limnology and Oceanography, 50, 923-929.
Bell, D. M. (2000) The ecology of coexisting Eleocharis species. PhD thesis, Botany
Department, University of New England, Armidale.
Bilton, D. T., Freeland, J. R. & Okamura, B. (2001) Dispersal in freshwater
invertebrates. Annual Review of Ecology and Systematics, 32, 159-181.
Boulton, A.J., Sheldon, F. & Jenkins, K.M. (2006) Natural disturbance and aquatic
invertebrates in desert rivers. In: Ecology of Desert Rivers (ed. R.T. Kingsford),
pp. 133-153. Cambridge University Press, Cambridge, UK.
Boulton, A.J. and Brock, M.A. (1999) Australian Freshwater Ecology: Processes and
Management. Gleneagles Publishing, Adelaide.
Brock, M.A., Capon, S.J. & Porter, J.L. (2006) Disturbance of plant communities
dependent on desert rivers. In: Ecology of Desert Rivers (ed. R.T. Kingsford),
pp. 100-132. Cambridge University Press, Cambridge, UK.
14
Brock, M. A., Nielsen, D. L., Shiel, R. J., Green, J. D. & Langley, J. D. (2003) Drought
and aquatic community resilience: the role of eggs and seeds in sediments of
temporary wetlands. Freshwater Biology, 48, 1207-1218.
Cain, M. L., Damman, H. & Muir, A. (1998) Seed dispersal and the Holocene migration
of woodland herbs. Ecological Monographs, 68, 325-347.
Charalambidou, I. & Santamaria, L. (2005) Field evidence for the potential of
waterbirds as dispersers of aquatic organisms. Wetlands, 25, 252-258.
Charalambidou, I. & Santamaría, L. (2002) Waterbirds as endozoochorous dispersers of
aquatic organisms: a review of experimental evidence. Acta OecologicaInternational Journal of Ecology, 23, 165-176.
Charalambidou, I., Santamaría, L. & Figuerola, J. (2003a) How far can the freshwater
bryozoan Cristatella mucedo disperse in duck guts? Archiv Fur Hydrobiologie,
157, 547-554.
Charalambidou, I., Santamaria, L., Jansen, C. & Nolet, B. A. (2005) Digestive plasticity
in Mallard ducks modulates dispersal probabilities of aquatic plants and
crustaceans. Functional Ecology, 19, 513-519.
Charalambidou, I., Santamaria, L. & Langevoord, O. (2003b) Effect of ingestion by five
avian dispersers on the retention time, retrieval and germination of Ruppia
maritima seeds. Functional Ecology, 17, 747-753.
Cottenie, K., Michels, E., Nuytten, N. & De Meester, L. (2003) Zooplankton
metacommunity structure: Regional vs. local processes in highly interconnected
ponds. Ecology, 84, 991-1000.
Crome, F. H. J. (1985) An experimental investigation of filter-feeding on zooplankton
by some specialized waterfowl. Australian Journal of Zoology, 33, 849-862.
Cross, J.W. (2006) Flowering and dormancy in duckweeds.
http://www.mobot.org/jwcross/duckweed/flowering-dormancy.htm, 15 July
2006.
Darwin C. (1859) On the Origin of Species by Means of Natural Selection. Murray,
London.
DWLBC (2005) Declared Plants in South Australia.
http://www.dwlbc.sa.gov.au/biodiversity/pests/weeds/plants_list.html, 11
January 2007.
Figuerola, J. & Green, A. J. (2002a) Dispersal of aquatic organisms by waterbirds: a
review of past research and priorities for future studies. Freshwater Biology, 47,
483-494.
Figuerola, J. & Green, A. J. (2002b) How frequent is external transport of seeds and
invertebrate eggs by waterbirds? A study in Donana, SW Spain. Archiv Fur
Hydrobiologie, 155, 557-565.
Figuerola, J., Green, A. J., Black, K. & Okamura, B. (2004) Influence of gut
morphology on passive transport of freshwater bryozoans by waterfowl in
Doñana (southwestern Spain). Canadian Journal of Zoology-Revue Canadienne
De Zoologie, 82, 835-840.
Figuerola, J., Green, A. J. & Santamaria, L. (2003) Passive internal transport of aquatic
organisms by waterfowl in Donana, south-west Spain. Global Ecology and
Biogeography, 12, 427-436.
Frisch, D., Green, A.J. & Figuerola, J. (2007) High dispersal capacity of a broad
spectrum of aquatic invertebrates via waterbirds. Aquatic Sciences. DOI
10.1007/s00027-007-0915-0
15
Green, A. J. & Figuerola, J. (2005) Recent advances in the study of long-distance
dispersal of aquatic invertebrates via birds. Diversity and Distributions, 11, 149156.
Green, A. J., Figuerola, J. & Sanchez, M. I. (2002) Implications of waterbird ecology
for the dispersal of aquatic organisms. Acta Oecologica-International Journal of
Ecology, 23, 177-189.
Green, A. J. & Sanchez, M. I. (2006) Passive internal dispersal of insect larvae by
migratory birds. Biology Letters, 2, 55-57.
Holt-Mueller, M. & Van der Valk, A. G. (2002) The potential role of ducks in wetland
seed dispersal. Wetlands, 22, 170-178.
Jenkins, K. M. & Boulton, A. J. (2003) Connectivity in a dryland river: short-term
aquatic microinvertebrate recruitment following floodplain inundation. Ecology,
84, 2708-2723.
Jenkins, K. M., Boulton, A. J. & Ryder, D. S. (2005) A common parched future?
Research and management of Australian arid-zone floodplain wetlands.
Hydrobiologia, 552, 57-73.
Jenkins, K.M. and Boulton, A.J. (2007) Detecting impacts and setting restoration targets
in arid-zone rivers: aquatic microinvertebrates responses to loss of floodplain
inundation. Journal of Applied Ecology, 44, 823-832.
King, A.J. (2004) Density and distribution of potential prey for larval fish in the main
channel of a floodplain river: pelagic versus epibenthic meiofauna. River
Research and Applications, 20(8), 883-897.
Kingsford, R. T., Curtin, A. L. & Porter, J. (1999) Water flows on Cooper Creek in arid
Australia determine "boom" and "bust" periods for waterbirds. Biological
Conservation, 88, 231-248.
Kingsford, R. T. & Johnson, W. (1998) Impact of water diversions on colonially-nesting
waterbirds in the Macquarie Marshes of arid Australia. Colonial Waterbirds, 21,
159-170.
Kingsford, R. T. & Norman, F. I. (2002) Australian waterbirds - products of the
continent's ecology. Emu, 102, 47-69.
Kingsford, R. T. & Thomas, R. F. (1995) The Macquarie Marshes in arid Australia and
their waterbirds: a 50-year history of decline. Environmental Management, 19,
867-878.
Langley, J. M., Shiel, R. J., Nielsen, D. L. & Green, J. D. (2001) Hatching from the
sediment egg-bank, or aerial dispersing? The use of mesocosms in assessing
rotifer biodiversity. Hydrobiologia, 446, 203-211.
Les, D. H., Crawford, D. J., Kimball, R. T., Moody, M. L. & Landolt, E. (2003)
Biogeography of discontinuously distributed hydrophytes: A molecular appraisal
of intercontinental disjunctions. International Journal of Plant Sciences, 164,
917-932.
Lowry, R. (2006) VassarStats. Fisher Exact Probability Test: 2x3.
http://faculty.vassar.edu/lowry/fisher2x3.html, 8 January 2007.
Marchant, S. & Higgins, P. J. (1990) Handbook of Australian, New Zealand and
Antarctic Birds. Melbourne: OUP.
Mellors, W. K. (1975) Selective predation of ephippial Daphnia and the resistance of
ephippial eggs to digestion. Ecology, 56, 974-980.
Mitchell, S. F. & Wass, R. T. (1995) Food-Consumption and Faecal Deposition of Plant
Nutrients by Black Swans (Cygnus atratus Latham) in a Shallow New-Zealand
Lake. Hydrobiologia, 306, 189-197.
16
Nogales, M., Quilis, V., Medina, F. M., Mora, J. L. & Trigo, L. S. (2002) Are predatory
birds effective secondary seed dispersers? Biological Journal of the Linnean
Society, 75, 345.
Paijmans, K. (1981) The Macquarie Marshes of inland northern New South Wales,
Australia. CSIRO Division of Land Use Research.
Pollux, B. J. A., Santamaria, L. & Ouborg, N. J. (2005) Differences in endozoochorous
dispersal between aquatic plant species, with reference to plant population
persistence in rivers. Freshwater Biology, 50, 232-242.
Powers, K. D., Noble, R. E. & Chabreck, R. H. (1978) Seed distribution by waterfowl in
southwestern Louisiana. Journal of Wildlife Management, 42, 598-605.
Proctor, V. W. 1964. Viability of crustacean eggs recovered from ducks. Ecology, 45,
656-658.
Renne, I. J., Gauthreaux, S. A. & Gresham, C. A. (2000) Seed dispersal of the Chinese
Tallow Tree (Sapium sebiferum (L.) Rosb.) by birds in coastal southern
California. American Midland Naturalist, 144, 202-215.
Roshier, D. A., Klomp, N. I. & Asmus, M. (2006) Movements of a nomadic waterfowl,
Grey Teal Anas gracilis, across inland Australia - results from satellite telemetry
spanning fifteen months. Ardea 94, 461–475.
Roshier, D. A., Robertson, A. I. & Kingsford, R. T. (2002) Responses of waterbirds to
flooding in an arid region of Australia and implications for conservation.
Biological Conservation, 106, 399-411.
Roshier, D. A., Robertson, A. I., Kingsford, R. T. & Green, D. G. (2001) Continentalscale interactions with temporary resources may explain the paradox of large
populations of desert waterbirds in Australia. Landscape Ecology, 16, 547-556.
Sánchez, M.I., Green, A.J., Amat, F. & Castellanos, E.M. (2007) Transport of brine
shrimps via the digestive system of migratory waders: dispersal probabilities
depend on diet and season. Marine Biology, 151, 1407–1415.
Sánchez, M.I., Green, A.J. & Castellanos, E.M. (2006) Internal transport of seeds by
migratory waders in the Odiel marshes, south-west Spain: consequences for
long-distance dispersal. Journal of Avian Biology, 37: 201-206.
Sawada, M., Viau, A. E. & Gajewski, K. (2003). The biogeography of aquatic
macrophytes in North America since the last glacial maximum. Journal of
Biogeography, 30, 999-1017.
StatSoft, (2001) Statistica 6.0. Tulsa, USA.
Tracey, J. P., Woods, R., Roshier, D., West, P. & Saunders, G. R. (2004) The role of
wild birds in the transmission of avian influenza for Australia: an ecological
perspective. Emu, 104, 109-124.
USDA-NRCS. (2007) The PLANTS database (http://plants.usda.gov, 11 January 2007).
National Plant Data Center, Baton Rouge, LA 70874-4490 USA.
Vandekerkhove, J., Declerck, S., Brendonck, L., Conde-Porcuna, J. M., Jeppesen, E. &
De Meester, L. (2005) Hatching of cladoceran resting eggs: temperature and
photoperiod. Freshwater Biology, 50, 96-104.
Welham, C. V. J. (1994) Flight speeds of migrating birds: a test of maximum range
speed predictions from three aerodynamic equations. Behavioural Ecology, 5, 18.
Western Australian Herbarium (1998) FloraBase, the Western Australian flora.
Department of Environment and Conservation. http://florabase.calm.wa.gov.au/,
11 January 2007.
17
Table 1 Emergence of invertebrates in inundated samples of waterbird faeces,
presenting numbers of samples for which each taxon was recorded on at least one of
five observation days. No invertebrates were recorded in controls (see text).
Grey teal
(n = 30)
Black swan
(n = 15)
Eurasian coot
(n = 15)
Total
(n=60)
Protozoans (ciliates)
Nematodes
Ostracods
Rotifers- Brachionus sp.
Unidentified bdelloid
Cephalodella sp.
25
1
2
0
0
0
7
3
1
0
1
0
13
9
5
2
2
1
45
13
8
2
3
1
Total
25
9
15
49
Invertebrate taxa
18
Table 2 Invertebrate propagules and live adults recorded in waterbird faecal samples when sieved. Listed are the number of samples with
propagules (n with eggs), the total number of propagules (Eggs) and the maximum number of propagules in any given sample (Max). Only
propagules that were apparently intact are included.
Propagule type
Grey Teal (n = 30)
____________________
n with eggs Eggs Max
Black Swan (n = 20)
______________________
n with eggs Eggs
Max
Australian
Eurasian Coot (n = 20)
Pelican (n = 1)
_______________________
____________
n with eggs
Eggs
Max
Eggs
Total (n = 71)
______________
n with eggs Eggs
Large branchiopod eggs
Ostracod eggs cf
Bryozoan statoblasts
Cladoceran ephippia
Live nematoda1
Other unidentified eggs (5 types)
15
22
1
4
-
56
84
1
7
-
10
13
1
3
-
2
10
6
3
5
2
83
21
3
15
1
36
10
1
9
4
17
14
4
2
1
4
141
32
6
4
1
1
22
7
3
3
1
12
261
3
12
0
11
22
50
22
12
2
7
74
569
57
28
4
27
Total
26
148
23
14
124
50
19
188
23
299
60
759
1
Adults, not propagules.
19
Table 3 Intact seeds and other plant diaspores of different mean length (mm) recorded in waterbird faecal samples. Shown are the number of
samples with apparently intact diaspores (WD), total number of diaspores (TD) and maximum number of diaspores in any given sample (Max).
Grey Teal
Black Swan
Eurasian Coot
Australian
Total (n = 71)
(n = 30)
(n = 20)
(n = 20)
Pelican (n = 1)
________________ _______________ _________________ ____________ _______________
Plant family
Plant species
Cyperaceae
Bolboschoenus fluviatilis
Eleocharis acuta
Eleocharis pallens
Eleocharis sphacelata
Schoenoplectus validus
Gramineae
Unidentified Poaceae
Juncaceae
Juncus sp.
Lemnaceae
Lemna disperma
Fabaceae
Medicago polymorpha1
Haloragaceae Myriophyllum crispatum
Characeae
Nitella sp.
Polygonaceae Polygonum arenastrum1
Ranunculaceae Ranunculus sceleratus 1
Portulaceae
Portulaca oleracea cf
Typhaceae
Typha dominguensis
Typha orientalis
Unknown
Unidentified (three taxa)
Total
1
Length
3
1.7
1.2
2.5
2.4
<1
<1
<1
1
0.5
<0.4
2.2
<1
1
<0.5
0.5
1-3
WD
TD
Max
WD
TD
Max
WD
TD
Max
TD
WD
19
4
1
1
3
1
3
3
9
2
8
1
2
81
21
2
1
4
1
3
3
40
4
12
1
2
19
18
2
1
2
1
1
1
16
2
4
1
1
1
1
1
1
3
2
1
1
2
4
6
2
1
1
2
4
4
1
1
7
1
2
-
1
14
1
2
-
1
7
1
1
-
1
3
38
2
3
69
-
26
175
26
7
16
7
8
18
9
116
19
4
1
1
3
2
3
5
1
18
4
1
8
1
2
6
4
TD Max
81
21
2
1
4
2
3
7
1
93
8
4
12
1
4
77
4
19
18
2
1
2
1
1
3
1
38
2
4
4
1
3
69
1
42 325
116
Alien species native to Europe.
20
Table 4 Viability of plant diaspores recorded in waterbird faecal samples. Shown are the total number of apparently intact diaspores (TD), the
number of diaspores that germinated (G) and the number that did not germinate but remained viable at the end of the study (V). All the other
diaspores were found to be rotten by the end of the germination trials (see methods).
Grey Teal
Black Swan
Eurasian Coot
Australian
(n = 30)
(n = 20)
(n = 20)
Pelican (n = 1)
________________ _______________ _________________ ____________
Plant family
Plant species
Cyperaceae
Bolboschoenus fluviatilis
Eleocharis acuta
Eleocharis pallens
Eleocharis sphacelata
Schoenoplectus validus
Gramineae
Unidentified Poaceae
Juncaceae
Juncus sp.
Lemnaceae
Lemna disperma
Fabaceae
Medicago polymorpha1
Haloragaceae Myriophyllum crispatum
Characeae
Nitella sp.
Polygonaceae Polygonum arenastrum1
Ranunculaceae Ranunculus sceleratus 1
Portulaceae
Portulaca oleracea cf
Typhaceae
Typha dominguensis
Typha orientalis
Unknown
Unidentified (three taxa)
Total
1
TD
G
V
TD
G
V
TD
G
V
TD
G
V
Total (n = 71)
_______________
TD
G
V
81
21
2
1
4
1
3
3
40
4
12
1
2
10
1
2
8
1
5
1
1
1
1
-
1
1
2
4
6
2
1
3
-
1
-
1
14
1
2
-
1
1
-
-
1
3
38
2
3
69
-
3
6
-
2
-
81
21
2
1
4
2
3
7
1
93
8
4
12
1
4
77
4
10
1
3
2
1
8
1
10
1
5
1
1
1
3
1
-
175
22
9
16
4
1
18
2
-
116
9
2
325
37
12
Alien species native to Europe.
21
Fig. 1 Cumulative percentage of samples from which invertebrates emerged during days
after inundating faeces of black swans, Eurasian coot and grey teal. See Table 1 for
more details.
Fig. 2 (a) Number of intact invertebrate propagules sieved from each faecal sample for
different waterbird species. Median number of propagules in any one sample was 1.5
for swans (n = 20), 9 for coot (n = 20) and 3 for teal (n = 30). (b) Number of
invertebrate taxa (see Table 2) recorded per sieved faecal sample for different waterbird
species. Medians were 1.5 taxa for swans, 2 for coot and 1 for teal.
Fig. 3 (a) Number of intact plant diaspores sieved from each faecal sample for different
waterbird species. Median number of diaspores in any one sample was 0 for swans (n =
20) and coot (n = 20) and 3.5 for teal (n = 30). (b) Number of plant taxa recorded (see
Table 3) per sieved faecal sample for different waterbird species. Medians were 0 for
swans and coot and 2 for teal.
22
Percentage
100
Swan
Protozoans
Coot
80
Teal
60
40
20
0
1 3 7 14 21
Percentage
100
1 3 7 14 21
1 3 7 14 21
1 3 7 14 21
1 3 7 14 21
1 3 7 14 21
1 3 7 14 21
1 3 7 14 21
1 3 7 14 21
Nematodes
80
60
40
20
0
1 3 7 14 21
Percentage
100
Ostracods
80
60
40
20
0
1 3 7 14 21
Percentage
100
Rotifers
80
60
40
20
0
1 3 7 14 21
Flood day
23
8
a)
Swan
Coot
Teal
Number of samples
7
6
5
4
3
2
1
0
0
1
2
3-5
6-9
10-14
15-24
25-50
Number of invertebrate propagules
14
b)
Swan
Coot
Teal
Number of samples
12
10
8
6
4
2
0
0
1
2
3
4
5
Number of invertebrate taxa
24
14
a)
Swan
Coot
Teal
Number of samples
12
10
8
6
4
2
0
0
1
2
3
4
5
6-10
11-15
16-26
Number of diaspores
14
b)
Swan
Coot
Teal
Number of samples
12
10
8
6
4
2
0
0
1
2
3
4
5
Number of plant taxa
25